Depolymerization-driven flow in nematode spermatozoa relates crawling speed to size and shape

Biophysical Journal

Volumn 94, Issue 10, 2008, Pages 3810-3823

  Zajac, Mark ^a   Dacanay, Brian ^b   Mohler, William A ^a   Wolgemuth, Charles W ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b University of Connecticut   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ANISOTROPY; ARTICLE; BIOLOGICAL MODEL; CAENORHABDITIS ELEGANS; CELL CULTURE; CELL SIZE; COMPUTER SIMULATION; CYTOLOGY; CYTOSKELETON; CYTOSOL; MALE; METHODOLOGY; MICROFLUIDICS; PHYSIOLOGY; SPERMATOZOON; SPERMATOZOON MOTILITY;

ANIMALS; ANISOTROPY; CAENORHABDITIS ELEGANS; CELL SIZE; CELLS, CULTURED; COMPUTER SIMULATION; CYTOSKELETON; CYTOSOL; MALE; MICROFLUIDICS; MODELS, BIOLOGICAL; SPERM MOTILITY; SPERMATOZOA;

EID: 43849109486     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.120980     Document Type: Article

References (87)

1. Huttenlocher, A., R. R. Sandborg, and A. F. Horwitz. 1995. Adhesion in cell-migration. Curr. Opin. Cell Biol. 7:697-706.
2. Lauffenburger, D., and A. F. Horwitz. 1996. Cell migration: a physically integrated molecular process. Cell. 84:359-369.
3. Mitchison, T. J., and L. P. Cramer. 1996. Actin based cell motility and cell locomotion. Cell. 84:371-379.
4. Rafelski, S. M., and J. A. Theriot. 2004. Crawling toward a unified model of cell motility: spatial and temporal regulation of actin dynamics. Annu. Rev. Biochem. 73:209-239.
5. Rodriguez, O. C., A. W. Schaefer, C. A. Mandato, P. Forscher, W. M. Bement, and C. M. Waterman-Storer. 2003. Conserved microtubuleactin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5:599-609.
6. Gracheva, M. E., and H. G. Othmer. 2004. A continuum model of motility in amoeboid cells. Bull. Math. Biol. 66:167-193.
7. Grimm, H. P., A. B. Verkhovsky, A. Mogilner, and J. J. Meister. 2003. Analysis of actin dynamics at the leading edge of crawling cells: implications for the shape of keratocyte lamellipodia. Eur. Biophys. J. Biophys. Lett. 32:563-577.
8. Bohnet, S., R. Ananthakrishnan, A. Mogilner, J. J. Meister, and A. B. Verkhovsky. 2006. Weak force stalls protrusion at the leading edge of the lamellipodium. Biophys. J. 90:1810-1820.
9. Marcy, Y., J. Prost, M. F. Carlier, and C. Sykes. 2004. Forces generated during actin-based propulsion: a direct measurement by micromanipulation. Proc. Natl. Acad. Sci. USA. 101:5992-5997.
10. Prass, M., K. Jacobson, A. Mogilner, and M. Radmacher. 2006. Direct measurement of the lamellipodial protrusive force in a migrating cell. J. Cell Biol. 174:767-772.
11. Svitkina, T. M., A. B. Verkhovsky, K. M. McQuade, and G. G. Borisy. 1997. Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J. Cell Biol. 139:397-415.
12. Verkhovsky, A. B., T. M. Svitkina, and G. G. Borisy. 1997. Contraction of actin-myosin II dynamic network drives cell translocation. Mol. Biol. Cell. 8:974.
13. Knecht, D. A., and W. F. Loomis. 1987. Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science. 237:1081-1085.
14. Laevsky, G., and D. A. Knecht. 2003. Cross-linking of actin filaments by myosin II Is a major contributor to cortical integrity and cell motility in restrictive environments. J. Cell Sci. 116:3761-3770.
15. Xu, X. X. S., E. Lee, T. L. Chen, E. Kuczmarski, R. L. Chishokn, and D. A. Knecht. 2001. During multicellular migration, myosin II serves a structural role independent of its motor function. Dev. Biol. 232:255-264.
16. Even-Ram, S., A. D. Doyle, M. A. Conti, K. Matsumoto, R. S. Adelstein, and K. M. Yamada. 2001. Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nat. Cell Biol. 11:63-80.
17. Janson, L. W., J. Kolega, and D. L. Taylor. 1991. Modulation of contraction by gelation/solation in a reconstituted motile model. J. Cell Biol. 114:1005-1015.
18. Janson, L. W., and D. L. Taylor. 1993. In vitro models of tail contraction and cytoplasmic streaming in amoeboid cells. J. Cell Biol. 123:345-356.
19. Bullock, T. L., A. J. McCoy, H. M. Kent, T. M. Roberts, and M. Stewart. 1998. Structural basis for amoeboid motility in nematode sperm. Nat. Struct. Biol. 5:184-189.
20. Roberts, T. M., and M. Stewart. 1997. Nematode sperm: amoeboid movement without actin. Trends Cell Biol. 7:368-373.
21. Miao, L., O. Vanderlinde, M. Stewart, and T. M. Roberts. 2003. Retraction in amoeboid cell motility powered by cytoskeletal dynamics. Science. 302:1405-1407.
22. Wolgemuth, C. W., L. Miao, O. Vanderlinde, T. Roberts, and G. Oster. 2005. MSP dynamics drives nematode sperm locomotion. Biophys. J. 88:2462-2471.
23. Charras, G. T., C. K. Hu, M. Coughlin, and T. J. Mitchison. 2006. Reassembly of contractile actin cortex in cell blebs. J. Cell Biol. 175: 477-490.
24. Cunningham, C. C. 1995. Actin polymerization and intracellular solvent flow in cell-surface blebbing. J. Cell Biol. 129:1589-1599.
25. Keller, H., A. D. Zadeh, and P. Eggli. 2002. Localized depletion of polymerized actin at the front of Walker carcinosarcoma cells increases the speed of locomotion. Cell Motil. Cytoskeleton. 53:189-202.
26. Yanai, M., C. M. Kenyon, J. P. Butler, P. T. MacKlem, and S. M. Kelly. 1996. Intracellular pressure is a motive force for cell motion in Amoeba proteus. Cell Motil. Cytoskeleton. 33:22-29.
27. Nelson, G., T. Roberts, and S. Ward. 1982. Caenorhabditis elegans spermatozoan locomotion: amoeboid movement with almost no actin. J. Cell Biol. 92:121-131.
28. Royal, D. C., M. A. Royal, D. Wessels, S. Lhernault, and D. R. Soll. 1997. Quantitative analysis of Caenorhabditis elegans sperm motility and how it is affected by mutants Spe11 and Unc54. Cell Motil. Cytoskeleton. 37:98-110.
29. Bottino, D. C., A. Mogilner, T. M. Roberts, and G. F. Oster. 2000. A computational model of crawling in Ascaris suum sperm. Mol. Biol. Cell. 11:380A.
30. Mogliner, A., and D. W. Verzi. 2003. A simple 1-D model for the crawling nematode sperm cell. J. Stat. Phys. 110:1169-1189.
31. Wolgemuth, C., A. Mogilner, and G. Oster. 2004. The hydration dynamics of polyelectrolyte gels with applications to drug delivery and cell motility. Eur. Biophys. J. 33:146-158.
32. Lamunyon, C. W., and S. Ward. 1998. Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc. R. Soc. Lond. Ser. B Biol. Sci. 265:1997-2002.
33. Ward,S.,E.Hogan,andG.A.Nelson.1983.The initiation of spermatogenesis in the nematode Caenorhabditis elegans. Dev. Biol. 98:70-79.
34. L'Hernault, S. W., and T. Roberts. 1995. Cell biology of nematode sperm. Methods Cell Biol. 48:273-301.
35. Nelson, G. A., and S. Ward. 1980. Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell. 19:457-464.
36. Cogswell, C. J., and C. J. R. Sheppard. 1991. Confocal differential interference contrast (DIC) microscopy: including a theoretical analysis of conventional and confocal DIC imaging. J. Microsc. 165:81-101.
37. Marganski, W. A., M. Dembo, and Y.-L. Wang. 2003. Measurements of cell-generated deformations on flexible substrata using correlation - based optical flow. Methods Enzymol. 361:197-211.
38. Roberts, T. M., F. M. Pavalko, and S. Ward. 1986. Membrane and cytoplasmic proteins are transported in the same organelle complex during nematode spermatogenesis. J. Cell Biol. 102:1787-1796.
39. Okada, Y., editor. 1998. Cell Volume Regulation: The Molecular Mechanism and Volume Sensing Machinery. Elsevier Science, Amsterdam, The Netherlands.
40. Strange, K. 1994. Cellular and Molecular Physiology of Cell Volume Regulation. CRC Press, Boca Raton, FL.
41. Buttery, S. M., G. C. Ekman, M. Seavy, M. Stewart, and T. M. Roberts. 2003. Dissection of the Ascaris sperm motility machinery identifies key proteins involved in Major Sperm Protein-based amoeboid locomotion. Mol. Biol. Cell. 14:5082-5088.
42. Italiano, J., Jr., T. M. Roberts, M. Stewart, and C. A. Fontana. 1996. Reconstruction in vitro of the motile apparatus from the amoeboid sperm of Ascaris shows that filament assembly and bundling move membranes. Cell. 84:105-114.
43. King, K. L., M. Stewart, and T. M. Roberts. 1994. Supramolecular assemblies of the Ascaris suum Major Sperm Protein (MSP) associated with amoeboid cell motility. J. Cell Sci. 107:2941-2949.
44. Baker, A. M. E., T. M. Roberts, and M. Stewart. 2002. 2.6 Angstrom resolution crystal structure of helices of the motile Major Sperm Protein (MSP) of Caenorhabditis elegans. J. Mol. Biol. 319:491-499.
45. Sepsenwol, S., H. Ris, and T. M. Roberts. 1989. A unique cytoskeleton associated with crawling in the amoeboid sperm of the nematode Ascaris suum. J. Cell Biol. 108:55-56.
46. Roberts, T. M., and M. Stewart. 2000. Acting like actin: the dynamics of the nematode Major Sperm Protein (MSP) cytoskeleton indicate a push-pull mechanism for amoeboid cell motility. J. Cell Biol. 149: 7-12.
47. Roberts, T. M., E. D. Salmon, and M. Stewart. 1998. Hydrostatic pressure shows that lamellipodial motility in Ascaris sperm requires membrane-associated Major Sperm Protein filament nucleation and elongation. J. Cell Biol. 140:367-375.
48. Italiano, J. E., M. Stewart, and T. M. Roberts. 1999. Localized depolymerization of the Major Sperm Protein cytoskeleton correlates with the forward movement of the cell body in the amoeboid movement of nematode sperm. J. Cell Biol. 146:1087-1095.
49. Leclaire, L. L., M. Stewart, and T. M. Roberts. 2003. A 48 KDa integral membrane phosphoprotein orchestrates the cytoskeletal dynamics that generate amoeboid cell motility in Ascaris sperm. J. Cell Sci. 116:2655-2663.
50. Evans, E., and A. Yeung. 1989. Apparent viscosity and cortical tension of blood granulocytes determined by micropipette aspiration. Biophys. J. 56:151-160.
51. Herant, M., W. A. Marganski, and M. Dembo. 2003. The mechanics of neutrophils: synthetic modeling of three experiments. Biophys. J. 84: 3389-3413.
52. Dai, J. W., H. P. Tingbeall, and M. P. Sheetz. 1997. The secretion-coupled endocytosis correlates with membrane tension changes in Rbl 2H3 cells. J. Gen. Physiol. 110:1-10.
53. Mogilner, A., and G. Oster. 2003. Shrinking gels pull cells. Science. 302:1340-1341.
54. Shibayama, M., and T. Tanaka. 1993. Volume phase transition and related phenomena of polymer gels. Adv. Polymer Sci. 109:1-62.
55. Bullock, T. L., T. M. Roberts, and M. Stewart. 1996. 2.5 Angstrom resolution crystal structure of the motile Major Sperm Protein (MSP) of Ascaris suum. J. Mol. Biol. 263:284-296.
56. Reference deleted in proof.
57. Tokita, T., and T. Tanaka. 1991. Friction coefficient of polymer networks of gels. J. Chem. Phys. 95:4613.
58. p) of the cell membrane of cultured glioma cells (C6). Acta Neurochir. Suppl. (Wien). 51: 11-13.
59. Kargol, A., M. Przestalski, and M. Kargol. 2005. A study of porous structure of cellular membranes in human erythrocytes. Cryobiology. 50:332-337.
60. Vargas, F. 1968. Filtration coefficient of the axon membrane as measured with hydrostatic and osmotic methods. J. Gen. Physiol. 51:13-27.
61. Garrick, R. A., T. G. Polefka, W. O. Cua, and F. P. Chinard. 1986. Water permeability of alveolar macrophages. Am. J. Physiol. Cell Physiol. 251:C524-C528.
62. 2+-dependent regulation of cell adhesiveness. J. Cell Sci. 118:369-379.
63. Pollard, T. D., L. Blanchoin, and R. D. Mullins. 2000. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 29:545-576.
64. Theriot, J. A., and T. J. Mitchison. 1991. Actin microfilament dynamics in locomoting cells. Nature. 352:126-131.
65. Watanabe, N., and T. J. Mitchison. 2002. Single-molecule speckle analysis of actin filament turnover in lamellipodia. Science. 295:1083-1086.
66. Mogilner, A., and L. Edelstein-Keshet. 2002. Regulation of actin dynamics in rapidly moving cells: a quantitative analysis. Biophys. J. 83:1237-1258.
67. Miyoshi, T., T. Tsuji, C. Higashida, M. Hertzog, A. Fujita, S. Narumiya, G. Scita, and N. Watanabe. 2006. Actin turnover-dependent fast dissociation of capping protein in the dendritic nucleation actin network: evidence of frequent filament severing. J. Cell Biol. 175:947-955.
68. Pantaloni, D. C. la Leinche, and M. F. Carlier. 2001. Cell biology-mechanism of actin-based motility. Science. 292:1502-1506.
69. du Roure, A., O. and Saez, A. Buguin, R. H. Austin, P. Chavrier, P. Siberzan, and B. Ladoux. 2005. Force mapping in epithelial cell migration. Proc. Natl. Acad. Sci. USA. 102:2390-2395.
70. Jurado, C., J. R. Haserick, and J. Lee. 2005. Slipping or gripping? Fluorescent speckle microscopy in fish keratocytes reveals two different mechanisms for generating a retrograde flow of actin. Mol. Biol. Cell. 16:507-518.
71. Burton, K., and J. Park. 1999. Keratocytes generate traction forces in two phases. Mol. Biol. Cell. 10:3745-3769.
72. Small, J. V., and G. P. Resch. 2005. The comings and goings of actin: coupling protrusion and retraction in cell motility. Curr. Opin. Cell Biol. 17:517-523.
73. McGrath, J. L., E. A. Osborn, Y. S. Tardy, C. F. Dewey, and J. H. Hartwig. 2000. Regulation of the actin cycle in vivo by actin filament severing. Proc. Natl. Acad. Sci. USA. 97:6532-6537.
74. Bereiter-Hahn, J. 2005. Mechanics of crawling cells. Med. Eng. Phys. 27:743-753.
75. Oster, G. 2002. Brownian ratchets: Darwin's motors. Nature. 417:25.
76. Loitto, V. M., T. Forslund, T. Sundqvist, K. E. Magnusson, and M. Gustafsson. 2002. Neutrophil leukocyte motility requires directed water influx. J. Leukoc. Biol. 71:212-222.
77. Joanny, J.-F., F. Jülicher, and J. Prost. 2003. Motion of an adhesive gel in a swelling gradient: a mechanism for cell locomotion. Phys. Rev. Lett. 90:168102.
78. Bottino, D., A. Mogilner, M. Stewart, and G. Oster. 2001. How nematode sperm crawl. J. Cell Sci. 115:367-384.
79. Rubinstein, B., K. Jacobson, and A. Mogilner. 2005. Multiscale two-dimensional modeling of a motile simple-shaped cell. Multiscale Model. Simul. 3:413-439.
80. King, K. L., J. Essig, T. M. Roberts, and T. S. Moerland. 1994. Regulation of the Ascaris Major Sperm Protein (MSP) cytoskeleton by intracellular pH. Cell Motil. Cytoskeleton. 27:193-205.
81. Drew, D. A., and L. A. Segel. 1971. Averaged equations for two phase flow. Stud. Appl. Math. 50:205-231.
82. Dembo, M., and F. Harlow. 1986. Cell motion, contractile networks, and the physics of interpenetrating reactive flow. Biophys. J. 50:109-121.
83. Vogel, S. 2003. Comparative Biomechanics: Life's Physical World. Princeton University Press, Princeton, NJ.
84. Tanaka, T., and D. Fillmore. 1979. Kinetics of swelling of gels. J. Chem. Phys. 70:1214-1218.
85. Osher, S., and R. Fedkiw. 2000. Level Set Methods and Dynamic Implicit Surfaces. Vol. 153, Applied Mathematical Sciences Series. Springer-Verlag, New York.
86. Sethian, J. A. 1999. Level Set Methods and Fast Marching Methods: Evolving Interfaces in Computational Geometry, Fluid Mechanics, Computer Vision and Material Science, 2nd Ed. Cambridge University Press, New York.
87. Schaff, J. C., B. M. Slepchenko, Y.-S. Choi, J. Wagner, D. Resasco, and L. M. Loew. 2001. Analysis of nonlinear dynamics on arbitrary geometries with the virtual cell. Chaos. 11:115-131.